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ORIGINAL RESEARCHSPINE
Comparison of Sagittal FSE T2, STIR, and T1-WeightedPhase-Sensitive Inversion Recovery in the Detection of Spinal
Cord Lesions in MS at 3TX P. Alcaide-Leon, X A. Pauranik, X L. Alshafai, X S. Rawal, X J. Oh, X W. Montanera, X G. Leung, and X A. Bharatha
ABSTRACT
BACKGROUND AND PURPOSE: Determining the diagnostic accuracy of different MR sequences is essential to design MR imagingprotocols. The purpose of the study was to compare 3T sagittal FSE T2, STIR, and T1-weighted phase-sensitive inversion recovery in thedetection of spinal cord lesions in patients with suspected or definite MS.
MATERIALS AND METHODS: We performed a retrospective analysis of 38 patients with suspected or definite MS. Involvement of thecervical and thoracic cord segments was recorded on sagittal FSE T2, STIR, and T1-weighted phase-sensitive inversion recovery sequencesindependently by 2 readers. A consensus criterion standard read was performed with all sequences available. Sensitivity, specificity, andinterobserver agreement were calculated for each sequence.
RESULTS: In the cervical cord, the sensitivity of T1-weighted phase-sensitive inversion recovery (96.2%) and STIR (89.6%) was significantlyhigher (P � .05) than that of FSE T2 (50.9%), but no significant difference was found between T1-weighted phase-sensitive inversionrecovery and STIR. In the thoracic cord, sensitivity values were 93.8% for STIR, 71.9% for FSE T2, and 50.8% for T1-weighted phase-sensitiveinversion recovery. Significant differences were found for all comparisons (P � .05). No differences were detected in specificity. Poorimage quality and lower sensitivity of thoracic T1-weighted phase-sensitive inversion recovery compared with the other 2 sequences wereassociated with a thicker back fat pad.
CONCLUSIONS: The use of an additional sagittal sequence other than FSE T2 significantly increases the detection of cervical and thoracicspinal cord lesions in patients with MS at 3T. In the cervical segment, both STIR and T1-weighted phase-sensitive inversion recovery offerhigh sensitivity and specificity, whereas in the thoracic spine, STIR performs better than T1-weighted phase-sensitive inversion recovery,particularly in patients with a thick dorsal fat pad.
ABBREVIATION: PSIR � T1-weighted phase-sensitive inversion recovery
MR imaging of the spinal cord is an important diagnostic
technique in MS because the prevalence of spinal cord ab-
normalities in patients with clinically isolated syndrome is as high
as 42%.1 In clinically diagnosed MS, spinal cord involvement
reaches 75%–92%, depending on the series.2-4 The presence of
asymptomatic cord lesions contributes to the demonstration of
dissemination in space in the McDonald 2010 criteria for MS, and
imaging of the spinal cord allows an increase of 18.3% in the
number of patients meeting the diagnostic criteria.5 The presence
of spinal cord lesions not only facilitates diagnosing MS but is also
predictive of conversion to clinically definite MS, especially in
patients with nonspinal clinically isolated syndrome who do not
fulfill brain MR imaging criteria.6 Moreover, spinal cord lesions
in MS can occur in isolation in 5% of patients, particularly in
primary-progressive MS.7
Spinal cord imaging is challenging because the spinal cord is a
small and mobile structure.8 In addition, its anatomic location
Received August 25, 2015; accepted after revision November 9.
From the Departments of Medical Imaging (P.A.-L., A.P., W.M., G.L., A.B.) and Move-ment Disorders (J.O.), St Michael’s Hospital, Toronto, Ontario, Canada; Departmentof Medical Imaging (L.A.), University Health Network, Mount Sinai Hospital,Toronto, Ontario, Canada; and Department of Medical Imaging (S.R.), UniversityHealth Network, Toronto Western Hospital, Toronto, Ontario, Canada.
Author contributions: guarantors of integrity of entire study: W.M., P.A.-L., A.B.;study concepts/study design or data acquisition or data analysis/interpretation:P.A.-L., L.A., A.P., G.L.; manuscript drafting or manuscript revision for importantintellectual content: all authors; approval of the final version of the manuscript: allauthors; literature research: P.A.-L.; statistical analysis: P.A.-L.; manuscript editing:P.A.-L., A.B., J.O.
This study was partially funded by Novartis in the form of an educational grant tosupport the fellowship training position for the first author (P.A.-L.). (Money paidto the institution.)
Please address correspondence to Paula Alcaide-Leon, MD, St Michael’s Hospital,Department of Medical Imaging, 30 Bond St, Toronto, ON M5B 1W8, Canada;e-mail: [email protected]
Indicates article with supplemental on-line table.
http://dx.doi.org/10.3174/ajnr.A4656
AJNR Am J Neuroradiol ●:● ● 2016 www.ajnr.org 1
Published January 21, 2016 as 10.3174/ajnr.A4656
Copyright 2016 by American Society of Neuroradiology.
makes it prone to ghosting artifacts caused by the heart and great
vessels as well as truncation artifacts. 3T MR imaging compared
with 1.5T is more prone to artifacts caused by B1 field inhomoge-
neity,9 susceptibility, vascular pulsation, and chemical shift.10,11
In addition, 3T MR imaging has a higher energy deposit within
the tissue, resulting in a higher specific absorption rate than lower
field scanners. These problems can be partially solved with vari-
ous technical adjustments and fast (parallel) imaging.12
Traditionally, the spinal cord in patients with MS has been
imaged by using sagittal and axial FSE T2/proton density se-
quences. Additional sequences, including STIR13,14 and T1 inver-
sion recovery,15 have shown promise by increasing lesion visibil-
ity, particularly at 3T, in which conventional FSE T2 and proton
density images are frequently unsatisfactory.16 STIR has proved
very useful as a complementary sequence in the detection of MS
lesions but cannot be used in isolation due to its lower specific-
ity.13,14 Numerous studies have demonstrated the superiority of
STIR over T2 at 1.5T,13,14,17-19 and 1 study15 also showed the
advantages of STIR at 3T in the cervical cord. To our knowledge,
no studies have been performed in the thoracic cord comparing
sagittal FSE T2 and STIR. A recent publication showed the advan-
tages of T1-weighted phase-sensitive inversion recovery (PSIR)
for the detection of cervical spinal cord lesions in MS at 3T.16 PSIR
has been shown to improve lesion localization and boundary def-
inition over STIR in the cervical spinal cord, but it has not been
tested in the thoracic cord.16
The aim of our study was to compare the sensitivity and spec-
ificity of sagittal STIR, PSIR, and FSE T2 in the detection of MS
spinal cord lesions at 3T, in both the cervical and thoracic
segments.
MATERIALS AND METHODSSubjectsApproval of the institutional review board to waive informed con-
sent was obtained for this retrospective study. Inclusion criteria
consisted of patients with definite or suspected MS who under-
went MR imaging of the spinal cord at 3T, including sagittal STIR,
PSIR, and FSE T2 as well as axial T2 sections in our institution
from July 1 to October 31, 2013. Exclusion criteria were a final
diagnosis of a disease causing spinal cord lesions different from
MS and substantial motion artifacts. Spinal MR imaging of 39
consecutive patients was reviewed. One patient with a final diag-
nosis of Churg-Strauss syndrome was excluded. Thirty-eight pa-
tients were included in the study. In 11 patients, only the cervical
segment was imaged, and in 12 patients, only the thoracic seg-
ment was covered. In 15 patients, both segments were included.
This inclusion resulted in 26 cervical and 27 thoracic spinal seg-
ments available for evaluation.
MR Imaging AcquisitionStudies were performed on a 3T MR imaging scanner (Magnetom
Skyra; Siemens, Erlangen, Germany) equipped with a 20-channel
head-neck coil and a 16-channel spine-array coil. Image parame-
ters are detailed in the Table. No contrast was administered before
performing these sequences.
Image AnalysisImages of all subjects were stripped of patient identifiers and
numbered randomly to facilitate blinded analysis. Two readers
(P.A.-L. and L.A., neuroradiologists with 6 years’ experience in
MR imaging) independently evaluated scans for the presence of
spinal cord lesions on each spinal cord level on sagittal PSIR,
sagittal STIR, and sagittal FSE T2 sequences. To facilitate this task
and improve consistency between readers, we drew lines separat-
ing the spinal cord levels across the midpoint of the intervertebral
disc, parallel to the vertebral endplates as shown in Fig 1C. These
reference lines were available during all readings. The upper limit
of the C1 segment was defined by the line connecting the tip of the
odontoid and the upper edge of the posterior arch of C1. The
lowest cord segment evaluated was T12, which was limited infe-
riorly by a line through the T12–L1 disc. Each sequence was eval-
uated independent of the other sequences so that the readers
could not use them to confirm or rule out the presence of a lesion.
Readings of different sequences for the same patient were sepa-
rated by at least a 2-week interval to avoid memory bias. Disagree-
ments were resolved by consensus. After the 2 independent read-
ings were completed and the disagreements were resolved, an
additional consensus reading was performed with all sequences
available. This was considered the criterion standard. Combined
information contained in sagittal FSE T2, proton density FSE,
PSIR, and STIR and in axial gradient-echo T2 of the cervical
spine and FSE T2 of the thoracic spine was taken into account
to decide which spinal cord segments truly had demyelinating
lesions and which were falsely identified as positive for demy-
elinating lesions due to the presence of artifacts. A lesion was
considered a true one if visible on at least 2 sequences, regard-
less of the imaging plane.
In our experience, PSIR images of the thoracic spine often
Acquisition parameters of MR imaging sequences
Segment Sequence PlaneFOV(mm)
AcquisitionMatrix
Thickness(mm) TR (ms) TE (ms) TI (ms)
No. of SignalsAcquired
Acquisition Time(min:sec)
ParallelImaging
Cervical PSIR Sagittal 220 320 � 224 3 2400 9.4 400 2 4:45 GRAPPA2Cervical STIR Sagittal 300 448 � 336 3 400 51 200 1 5:46 GRAPPA2Cervical FSE PD Sagittal 220 320 � 288 3 2500 23 1 2:02 NoneCervical FSE T2 Sagittal 220 384 � 307 3 3500 106 2 3:35 NoneCervical GE T2 Transverse 180 256 � 218 3 740 17 2 4:25 GRAPPA2Thoracic PSIR Sagittal 330 384 � 269 3 2400 9.5 400 2 4:45 GRAPPA2Thoracic STIR Sagittal 330 448 � 336 3 4000 50 200 1 5:46 GRAPPA2Thoracic FSE PD Sagittal 330 320 � 288 3 2500 21 1 4:02 NoneThoracic FSE T2 Sagittal 330 448 � 336 3 4000 96 1 4:26 NoneThoracic FSE T2 Transverse 180 256 � 176 5 6780 107 2 4:46 None
Note:—GE indicates gradient-echo; PD, proton density; GRAPPA, generalized autocalibrating partially parallel acquisition.
2 Alcaide-Leon ● 2016 www.ajnr.org
have very poor quality, particularly in patients with a large
thoracoabdominal diameter. To confirm our hypothesis that
patient size affects PSIR sequence quality in the thoracic spine,
we classified images by consensus into 2 groups: good quality
or poor quality on the basis of noise and CSF signal saturation.
We also measured the thickness of the dorsal back fat pad on
PSIR sequences of the thoracic region. This was used as a sur-
rogate marker of the thoracoabdominal diameter, which could
not be measured directly on the images. This evaluation was
performed by 1 author (P.A.-L.) in the midline at the level of
T1–T2, T8 –T9, and L1–L2. The mean of the 3 values was cal-
culated. Thicknesses of the back fat pad of patients with good-
quality and poor-quality PSIR of the thoracic spine were
compared.
Statistical AnalysisInterrater reliability analysis by the Cohen � coefficient was per-
formed to determine segmental lesion detection consistency
among raters. � values were interpreted on the basis of the con-
vention by Landis and Koch.20
Estimates of sensitivity and specificity were calculated for each
sequence in the cervical and thoracic segments (On-line Table).
To perform the calculation, we summated all false-positive, false-
negative, true-positive, and true-negative segments of the differ-
ent patients. Thus, calculated values of sensitivity and specificity
do not represent directly the accuracy of the sequence in diagnos-
ing MS but do represent the accuracy of the sequence in distin-
guishing an affected and nonaffected segment of the cord. Confi-
dence intervals for sensitivity and specificity were produced with
the Wilson score method.21 Accuracy of the sequences was also
calculated.
Mean thickness of the thoracic back fat pad of the good-
quality and poor-quality groups was compared by using the
Mann-Whitney U test. The Pearson
correlation coefficient was used to as-
sess correlations between the thickness
of the back fat pad and the sensitivity
of the sagittal PSIR of the thoracic
spine.
RESULTSTwenty-six female and 12 male subjects
were included (mean age, 42.1 years;
range, 25– 68 years). Of 38 subjects in-
cluded in the study, 33 had clinically def-
inite MS (n � 26, relapsing-remitting
MS; n � 3, primary-progressive MS; n �
3, secondary-progressive MS; and n � 1,
progressive-relapsing MS). The mean
disease duration was 9 years (range,
1–27 years). The remaining 5 subjects
included 2 patients with clinically iso-
lated syndrome, 1 patient with radiolog-
ically isolated syndrome, and 2 patients
with vague sensory symptoms without a
definite clinically isolated syndrome.
There were no exclusions due to mo-
tion artifacts. As per criterion standard
evaluation (consensus reading with all sequences available), spi-
nal cord lesions were present in 84% of the cervical examinations
and in 85% of the thoracic segments. In 6 patients, the upper
thoracic region was not included in the FOV; thus, 8 thoracic
segments could not be evaluated. One hundred eighty-two cervi-
cal and 316 thoracic spinal cord segments were evaluated. Of
these, 106 cervical and 128 thoracic segments were affected by MS
lesions. The number of true-positive, true-negative, false-posi-
tive, and false-negative spinal cord segments and the sensitivity,
specificity, accuracy, and � coefficient of each sagittal sequence
are shown in the On-line Table. Comparisons among the number
of true-positive, false-negative, and false-positive spinal cord seg-
ments of the 3 different sagittal sequences in the cervical and tho-
racic segments are shown in Fig 2. In the cervical region, the sen-
sitivity of STIR and PSIR was significantly higher than that of FSE
T2 (P � .05) (Fig 1). No significant difference was found in
sensitivity between PSIR and STIR in the cervical region. In the
thoracic region, the sensitivity of STIR was significantly higher
than that of FSE T2 and PSIR, and the sensitivity of FSE T2 was
significantly higher than that of PSIR (P � .05). Specificities of
all cervical and thoracic sagittal sequences studied were very
similar, with no significant differences identified. Interob-
server agreement was higher for STIR than for FSE T2 and
PSIR, in both the cervical and thoracic segments.
At visual inspection, all sequences were rated as good quality
except for 10 PSIR thoracic studies that showed inhomogeneous
CSF saturation and increased noise (Fig 3). The distribution of the
variable “size of the back fat pad” in the good-quality and poor-
quality groups is shown in Fig 3E. Back fat pad thickness in the
poor-quality group was significantly higher compared with the
high-quality group (P � .001). The mean back fat pad thickness
was 13 mm (95% CI, 9.9 –16.1 mm) in the good-quality group
FIG 1. Sagittal PSIR (A), FSE T2 (B), and STIR (C) sequences in a patient with MS. A demyelinatinglesion at the C2 level (arrows) is adequately visualized on PSIR (A) and STIR (C) but not on FSE T2(B). C, An example of reference lines through the center on the disc spaces used to separate thevertebral levels (gray lines).
AJNR Am J Neuroradiol ●:● ● 2016 www.ajnr.org 3
and 24.6 mm (95% CI, 21.8 –27.3 mm)
in the poor-quality group. A moderate
negative correlation (Fig 3F) was found
between the thickness of the back fat pad
and the sensitivity of the sagittal PSIR
sequence of the thoracic spine (r �
�0.58, P � .003).
DISCUSSIONThis study shows that lesion detection in
the cervical region is lower on sagittal
FSE T2 than on PSIR and STIR. The sen-
sitivity of sagittal PSIR in our sample was
slightly higher than that of STIR; how-
ever, the differences were not signifi-
cant. In the thoracic spine, lesion detec-
tion of STIR was significantly better than
that of FSE T2 and PSIR and lesion de-
tection of FSE T2 was significantly better
than that of PSIR.
The poor performance of PSIR in the
thoracic region appears to be related to
the thickness of the back fat pad. We are
unsure about the cause of this effect in
large patients. One explanation may be
the dielectric effect. When the abdomi-
nal diameter exceeds the radiofrequency
wavelength, the 180° pulse is not homo-
geneous through the FOV. Therefore,
some areas may be getting an inversion
pulse different from 180°. This effect,
however, should also be detected on
STIR because both are inversion recov-
ery sequences. Another possibility may
be a problem in phase unwrapping be-
cause the generation of true phase-sen-
sitive images requires phase images to be
FIG 2. Stacked bar charts show the total number of true-positive, false-negative, and false-positive spinal cord segments in the cervical (A) andthoracic (B) regions on the 3 different sagittal sequences evaluated. The horizontal lines represent the total number of segments truly affectedby lesions as per criterion standard evaluation.
FIG 3. A, Thoracic sagittal PSIR image of a patient with MS with a thick back fat pad showsincreased noise and failure of CSF suppression. A demyelinating lesion (white arrow) is clearlyidentified on STIR (B) but not seen on PSIR (A). Sagittal PSIR (C) and STIR (D) sequences of aslim patient with MS show adequate contrast between the lesions (arrow caps) and the cordand adequate CSF signal suppression on PSIR. E, The boxplot shows the distribution of thevariable thickness of the back fat pad in the group of patients with good- and poor-qualitythoracic PSIR images. The bottom and the top of the boxes represent the 25th and 75thpercentiles, respectively; the median is represented by the horizontal line in the box; and therange corresponds to the whiskers that extend from the box. Patients with poor-quality PSIRsequences of the thoracic spine have a median back fat pad size significantly thicker than thatin patients with good-quality images. F, The scatterplot shows the negative correlationbetween the sensitivity of the PSIR sequence of the thoracic segment and the thickness ofthe back fat pad (r � �0.53).
4 Alcaide-Leon ● 2016 www.ajnr.org
unwrapped first.22 The algorithm for phase unwrapping depends
on a smooth variation in phase, and this constraint is sometimes
not met, depending on the patient’s anatomy. A similar problem
was found by Riederer et al23 when using a double inversion re-
covery sequence in the cervical cord. They excluded 10% of their
sample due to artifacts presumably caused by adiposity. We did
not observe this problem in the cervical examinations, but we
found it in 37% of our thoracic examinations. We decided not to
exclude large patients with poor image quality because our inten-
tion was to test sequences as they would be used in the routine
clinical practice. Our observation is noteworthy because a se-
quence that provides suboptimal image quality in 37% of the
patients would not be adequate for routine clinical use; thus, the
utility of PSIR to detect thoracic spinal cord lesions may be
limited.
Conventionally, sagittal FSE T2 is the most commonly used
sequence when imaging the spinal cord in MS. Our results suggest
that the use of an additional sagittal sequence can significantly
increase the detection of MS lesions in the cervical and thoracic
cord without a substantial decrease in specificity. Both sagittal
PSIR and STIR perform well in this regard in the cervical spine,
but only STIR appears to be adequate in the thoracic region. All
the sequences studied have reasonable scanning times and can be
implemented in routine clinical practice, but there is a small ad-
vantage for cervical PSIR because it is 1 minute shorter than STIR
with our acquisition parameters.
We used a segment-based approach to quantify affected spinal
cord tissue. With this method, interobserver agreement was mod-
erate for PSIR and FSE T2 of the thoracic spine, substantial for
FSE T2 and PSIR of the cervical spine and for STIR of the thoracic
spine, and almost perfect for STIR of the cervical spine. Studies
comparing lesion detection of different sequences in the spinal
cord often had a consensus read16,24 and a single read25 or did
not report � values.14,18,19 Of note, our � values using a seg-
ment-based approach to quantify spinal cord lesion load are
higher than those reported in prior studies13,26 that used lesion
count; this finding suggests that a segment-based approach
may be a more reliable way to quantify lesion burden in the
spinal cord in MS.
The results of our study provide useful information for the
design of 3T MR imaging protocols in MS. The superiority of
STIR over T2 at 1.5T has been demonstrated on prior studies.14,19
Dietemann et al25 reported that the use of STIR in addition to
sagittal T2 in the spinal cord increases the number of MS lesions
detected by 46%. Another study by Nayak et al,26 which included
a variety of scans performed at 1.5T and 3T, showed a 35% in-
crease in the number of lesions detected using STIR compared
with conventional sagittal T2. At 3T, Poonawalla et al16 reported
improved lesion detection of sagittal STIR over sagittal FSE T2;
however, the sample was small (n � 12) and no statistical analyses
were performed to support the findings. In the study by Philpott
and Brotchie,15 sagittal STIR showed a statistically significant in-
crease in cervical cord lesion detection compared with FSE T2 at
3T. Our findings, therefore, are in agreement with previous stud-
ies at 1.5T and 3T that have shown that sagittal T2 alone does not
have adequate sensitivity to detect cervical cord lesions (Fig 1),
supporting the need to incorporate alternative sequences with
higher sensitivity to accurately detect cervical cord lesions in MS.
We have also demonstrated the utility of STIR sequences for im-
proving spinal cord lesion detection in the thoracic segment at 3T,
which has not been assessed in detail in prior studies.
Our findings support the use of PSIR as another alternative to
improve the detection of MS lesions in the cervical spinal cord. In
our study, PSIR was not superior to STIR in lesion detection in the
cervical spine. Prior studies comparing these 2 sequences include
the work by Poonawalla et al16 (cervical STIR versus PSIR) and
Philpott and Brotchie15 (cervical T1 inversion recovery without
phase reconstruction versus STIR); in both cases, samples were
very small (n � 12 and n � 11, respectively) and statistical analysis
of lesion detection was not performed. Thus, the existing litera-
ture does not provide enough evidence regarding the comparison
between PSIR and STIR in the cervical cord, though a trend to-
ward PSIR superiority has been observed, as in our study.
Our results raise the question of whether sagittal T2 should be
included in the cervical examinations of patients with MS at 3T,
given its inferiority compared with other sequences. We have
shown the advantage of substituting sagittal T2 with STIR or PSIR
in terms of cervical cord lesion detection; however, we have not
evaluated the impact of eliminating sagittal T2 in the character-
ization of nondemyelinating cord pathologies and incidental
findings.
This study has a number of limitations. First, we used a
segment-based lesion-quantification approach in which the
only information recorded was the presence or lack of lesions
in each cord segment. Although this method showed substan-
tially better interobserver agreement than lesion count, it has
the disadvantage of being insensitive to differential lesion bur-
den within a particular segment. Second, we focused on com-
paring FSE T2, STIR, and PSIR, but recent studies have dem-
onstrated that double inversion recovery23 and T1 MPRAGE24
can be applied in the cervical cord of patients with MS; how-
ever, their long acquisition time (�7 minutes) limits their ap-
plication in routine clinical practice. Due to the retrospective
nature of our study, we did not have these sequences available
for analysis in our study population, but future studies com-
paring T1-weighted phase-sensitive inversion recovery and T1
MPRAGE with STIR and PSIR would be useful. Third, contrary
to prior studies, we did not calculate the body mass index.23
This parameter is easy to calculate and would allow rapid pr-
escanning decision-making for STIR versus PSIR.
CONCLUSIONSOur results suggest that at 3T, an additional sequence other than
sagittal FSE T2 should be incorporated to improve lesion detec-
tion in the spinal cord of patients with MS. In the cervical cord,
both sagittal STIR and PSIR showed significantly better lesion
detection than sagittal FSE T2. In contrast, in the thoracic spinal
cord, the sensitivity of PSIR is markedly worse than that of STIR
and FSE T2, particularly in large patients, and STIR is clearly
superior to FSE T2. These findings should be taken into account
when planning sequence protocols to optimize lesion detection in
the spinal cord in MS.
AJNR Am J Neuroradiol ●:● ● 2016 www.ajnr.org 5
ACKNOWLEDGMENTSWe would like to thank Bart Schraa, Siemens Application Sup-
port, for his help with the technical aspects of this manuscript.
Disclosures: Paula Alcaide-Leon—RELATED: Grant: Novartis.* Sapna Rawal—UNRELATED: Travel/Accommodations/Meeting Expenses Unrelated to ActivitiesListed: Association of University Radiologists–GE Radiology Research Academic Fel-lowship Award, Comments: I am a recipient of the Association of University Radi-ologists–GE Radiology Research Academic Award for 2015, and the sponsoring bodypaid for my travel expenses to the Association of University Radiologists meeting inApril 2015. Jiwon Oh—UNRELATED: Consultancy: Biogen-Idec, Novartis, Teva, Gen-zyme, EMD Serono, Roche; Grants/Grants Pending: Biogen-Idec, Genzyme, MultipleSclerosis Society of Canada*; Payment for Lectures (including service on SpeakersBureaus): EMD Serono, Novartis, Genzyme, Teva, Biogen-Idec; Travel/Accommoda-tions/Meeting Expenses Unrelated to Activities Listed: Genzyme, EMD Serono. Gen-eral Leung—UNRELATED: Grants/Grants Pending: University of Toronto,* Com-ments: Internal funding was received for a project for carotid atherosclerosisimaging; Patents (planned, pending or issued): operation of wireless devices throughthe Faraday Cage,* inhibition of intraplaque hemorrhage using drug therapy*; Other:In-kind support was received from Siemens, Synaptive Medical, VisualSonics/Fuji-film. Aditya Bharatha—RELATED: Grant: Novartis,* Comments: educational grant tosupport research fellow (first author, P.A.-L.); UNRELATED: Payment for Lectures(including service on Speakers Bureaus): EMD Serono, Novartis, Biogen, Comments:honoraria for educational lectures on MS. *Money paid to the institution.
REFERENCES1. Brex PA, O’Riordan JI, Miszkiel KA, et al. Multisequence MRI in
clinically isolated syndromes and the early development of MS.Neurology 1999;53:1184 –90 CrossRef Medline
2. Ikuta F, Zimmerman HM. Distribution of plaques in seventy au-topsy cases of multiple sclerosis in the United States. Neurology1976;26:26 –28 CrossRef Medline
3. Nijeholt GJ, van Walderveen MA, Castelijns JA, et al. Brain and spi-nal cord abnormalities in multiple sclerosis: correlation betweenMRI parameters, clinical subtypes and symptoms. Brain 1998;121(pt 4):687–97 CrossRef Medline
4. Bot JC, Barkhof F, Lycklama a Nijeholt G, et al. Differentiation ofmultiple sclerosis from other inflammatory disorders and cerebro-vascular disease: value of spinal MR imaging. Radiology 2002;223:46 –56 CrossRef Medline
5. Bot JC, Barkhof F, Polman CH, et al. Spinal cord abnormalities inrecently diagnosed MS patients: added value of spinal MRI exami-nation. Neurology 2004;62:226 –33 CrossRef Medline
6. Sombekke MH, Wattjes MP, Balk LJ, et al. Spinal cord lesions inpatients with clinically isolated syndrome: a powerful tool in diag-nosis and prognosis. Neurology 2013;80:69 –75 CrossRef Medline
7. Thorpe JW, Kidd D, Moseley IF, et al. Spinal MRI in patients withsuspected multiple sclerosis and negative brain MRI. Brain 1996;119(pt 3):709 –14 CrossRef Medline
8. Mikulis DJ, Wood ML, Zerdoner OA, et al. Oscillatory motion of thenormal cervical spinal cord. Radiology 1994;192:117–21 CrossRefMedline
9. Yang QX, Wang J, Zhang X, et al. Analysis of wave behavior in lossydielectric samples at high field. Magn Reson Med 2002;47:982– 89CrossRef Medline
10. Phalke VV, Gujar S, Quint DJ. Comparison of 3.0 T versus 1.5 T MR:
imaging of the spine. Neuroimaging Clin N Am 2006;16:241– 48, ixMedline
11. Fries P, Runge VM, Kirchin MA, et al. Magnetic resonance imagingof the spine at 3 Tesla. Semin Musculoskelet Radiol 2008;12:238 –52CrossRef Medline
12. Filippi CG, Carlson M, Johnson JM, et al. Improvements in lumbarspine MRI at 3 T using parallel transmission. AJR Am J Roentgenol2012;199:861– 67 CrossRef Medline
13. Bot JC, Barkhof F, Lycklama a Nijeholt GJ, et al. Comparison of aconventional cardiac-triggered dual spin-echo and a fast STIR se-quence in detection of spinal cord lesions in multiple sclerosis. EurRadiol 2000;10:753–58 CrossRef Medline
14. Hittmair K, Mallek R, Prayer D, et al. Spinal cord lesions in patientswith multiple sclerosis: comparison of MR pulse sequences. AJNRAm J Neuroradiol 1996;17:1555– 65 Medline
15. Philpott C, Brotchie P. Comparison of MRI sequences for evalua-tion of multiple sclerosis of the cervical spinal cord at 3 T. Eur JRadiol 2011;80:780 – 85 CrossRef Medline
16. Poonawalla AH, Hou P, Nelson FA, et al. Cervical spinal cord lesionsin multiple sclerosis: T1-weighted inversion-recovery MR imagingwith phase-sensitive reconstruction. Radiology 2008;246:258 – 64CrossRef Medline
17. Rocca MA, Mastronardo G, Horsfield MA, et al. Comparison of threeMR sequences for the detection of cervical cord lesions in patientswith multiple sclerosis. AJNR Am J Neuroradiol 1999;20:1710 –16Medline
18. Campi A, Pontesilli S, Gerevini S, et al. Comparison of MRI pulsesequences for investigation of lesions of the cervical spinal cord.Neuroradiology 2000;42:669 –75 CrossRef Medline
19. Mascalchi M, Dal Pozzo G, Bartolozzi C. Effectiveness of the short TIinversion recovery (STIR) sequence in MR imaging of intramedul-lary spinal lesions. Magn Reson Imaging 1993;11:17–25 CrossRefMedline
20. Landis JR, Koch GG. The measurement of observer agreement forcategorical data. Biometrics 1977;33:159 –74 CrossRef Medline
21. Julious SA. Two-sided confidence intervals for the single proportion:comparison of seven methods by Robert G. Newcombe, Statistics inMedicine 1998;17:857– 872. Stat Med 2005;24:3383–84 Medline
22. Moran PR, Kumar NG, Karstaedt N, et al. Tissue contrastenhancement: image reconstruction algorithm and selection of TIin inversion recovery MRI. Magn Reson Imaging 1986;4:229 –35CrossRef Medline
23. Riederer I, Karampinos DC, Settles M, et al. Double inversion recov-ery sequence of the cervical spinal cord in multiple sclerosis andrelated inflammatory diseases. AJNR Am J Neuroradiol 2015;36:219 –25 CrossRef Medline
24. Nair G, Absinta M, Reich DS. Optimized T1-MPRAGE sequencefor better visualization of spinal cord multiple sclerosis lesionsat 3T. AJNR Am J Neuroradiol 2013;34:2215–22 CrossRef Medline
25. Dietemann JL, Thibaut-Menard A, Warter JM, et al. MRI in multiplesclerosis of the spinal cord: evaluation of fast short-tau inversion-recovery and spin-echo sequences. Neuroradiology 2000;42:810 –13CrossRef Medline
26. Nayak NB, Salah R, Huang JC, et al. A comparison of sagittal shortT1 inversion recovery and T2-weighted FSE sequences for detectionof multiple sclerosis spinal cord lesions. Acta Neurol Scand 2014;129:198 –203 CrossRef Medline
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